Super-Charged Gills and Blood

We all know that people need oxygen to live, but few of us understand
why. The reason has to do with chemical properties of oxygen itself. Oxygen
has a remarkably high affinity for electrons, those tiny, negatively charged
particles zipping around atomic nuclei in discrete orbitals. Oxygen is so
'greedy' for electrons because each atom is only two electrons short of
having a full outer orbit, which is a lower, more stable energy state than
remaining not-quite full. In order to become more stable, oxygen 'steals'
outer orbital electrons from other atoms less able to hold onto them than
itself. In living things, this electron theft occurs within tiny cellular
organelles called mitochondria. The actual process is a complex cascade of
electrons changing possession from one intermediate molecule to another and
takes place on the highly folded internal membrane of mitochondria. At
virtually every stage of this highly coordinated electron shuffle — which
ultimately packages energy in the form of a chemical called ATP that is
easily handled by living cells — oxygen, either acting alone or as part of
other molecules, is the chief instigator. Essentially, the force with which
oxygen rips away electrons from other atoms within mitochondria is what
powers all multicellular life, including human beings and Great White
Sharks.

The major function of the respiratory system of any animal is the
exchange of oxygen and carbon dioxide (CO2) between the environment and
metabolizing cells. We humans and other terrestrial animals that breathe air
inhabit a veritable ocean of oxygen: some 21% of the atmosphere is composed
of oxygen gas (O2, because, in the absence of other elements from which to
steal electrons, an atom of oxygen will share with another of its kind). In
contrast, aquatic animals — which need oxygen just as much as we do — must
contend with much lower concentrations of this precious gas. Because the
amount of dissolved gas a liquid can hold depends on its temperature, the
ocean contains a maximum of about 4.5% oxygen in very cold water to a
minimum of almost 0% in very warm water. Some aquatic animals reduce their
total oxygen demand by remaining small or inactive or both. But a large,
active marine animals like the White Shark must work hard to wrest enough
oxygen from the sea to power its needs.

The first step is getting the oxygen-bearing medium to the actual site of
gas exchange. Like many active sharks, the Great White relies largely on
'ram jet' ventilation — its own forward movement forcing water into the
mouth, through the throat, and out the gill slits. But the White Shark may
also employ a weak pumping action, contracting its pharyngeal (throat) and branchial (gill) muscles in a front-to-back sequence to help draw water into
the mouth and squeeze it out the gills. This is the same rearward sequence
of muscular contractions — albeit, performed rather more strongly — that
allow certain bottom-dwelling sharks to lie on the substrate for extended
periods. To the best of my knowledge, no one has observed a White Shark
lying on the bottom, and this species relatively weak pharyngobranchial
muscles may make it impossible to do so. Thus, the White Shark may be
condemned to a life of perpetual motion, gasping for what little dissolved
oxygen its gills can extract from the medium through which it swims.

As in other sharks, the Great White's gill filaments provide a relatively
large surface for gas exchange. Of the White Shark's five gill arches, the
first supports only a single row of gill filaments, while the remaining four
support double rows. Each of the second through fifth gill arches supports a
sheet of muscular and connective tissue (supported by cartilaginous gill
rays) called a septum. Each septum — in turn — supports a row of gill
filaments on either side, extending beyond them to form a flap over each
gill slit. Some relatively inactive sharks and batoids (skates and rays)
possess behind each eye an accessory respiratory organ called a spiracle,
but this organ is minute or absent in the White Shark which relies
exclusively on gill filaments to supply its respiratory needs. Along the top
and bottom of each gill filament are delicate, closely-packed, transverse
flaps of gill tissue known as secondary lamellae. It is these lamellae that
are the actual sites of gas exchange in the Great White and other sharks.
Each lamella is equipped with tiny arteries that carry blood in a direction
opposite to that of the water flowing over them.

This counter-current flow brings oxygen-poor, carbon dioxide-laden blood
in continual contact with fresh, carbon dioxide-poor, oxygen-rich seawater.
Thus, the counter-current flow of blood and seawater maintains a steep
concentration gradient, fostering the efficient diffusion of carbon dioxide
out of the blood and oxygen in. When the blood holds an elevated
concentration of carbon dioxide (diffused into the bloodstream as a waste
product of cellular metabolism), it becomes slightly acidic and less able to
hold onto the oxygen component of this gas, which then easily diffuses out
of the blood at the gills. The blood's acidity thus reduced, oxygen can now
diffuse from the seawater to the shark's blood via the gill filaments. To
compensate for the relatively low concentration of dissolved oxygen in
seawater, water passes over the secondary lamellae of sharks some 20 times
more slowly than air remains in contact with the equivalent gas exchange
sites (alveoli of the lungs) in humans. This delay allows sufficient time
for dissolved oxygen to diffuse into a shark's blood.

Blood is a unique tissue in that it is largely liquid, composed of blood
cells swept along in a viscous fluid called serum. As in humans, sharks have
two basic types of blood cell, white and red. White blood cells are
primarily involved in the body's immunological defense against foreign
invaders (such as disease-causing microbes), while red blood cells are the
main carriers of respiratory gases. In sharks, red blood cells are formed in
the spleen (as they are in humans) and a peculiar structure in the esophagus
called Leydig's organ (which is unique to elasmobranchs and seems to also
play a role in the shark immune system). Unlike that of all non-mammalian
vertebrates, shark red blood cells are nucleated and thus contain the
genetic material DNA. (Pity there seems to be no undersea equivalent of a
prehistoric blood-sucking insect preserved in amber, otherwise we could
clone Megalodon and find out — once and for all — what this extinct
mega-toothed shark looked like in life.) However, as in human blood, the
primary oxygen and carbon-dioxide carrying molecule in shark blood is hemoglobin.

Sharks typically have larger and fewer red blood cells than teleosts, and
thus must deal with longer average gas diffusion distances, making oxygen
uptake at the gills less efficient. In order to compensate for this
logistical hurdle, shark hemoglobin has a tremendous affinity for oxygen,
becoming saturated at a partial pressure some 200% lower than that required
by most teleosts. Perhaps most intriguing is the discovery that in certain
egg-laying sharks, such as the Swell Shark (Cephaloscyllium ventriosum),
fetal hemoglobin has a higher oxygen affinity than adult hemoglobin,
possibly to allow for more efficient oxygen extraction from the relatively
stagnant water within the egg case. A similarly enhanced oxygen-binding
ability in fetal White Sharks may permit rapid growth in a womb that may be
shared by as many as 11 oxygen-needy, carbon dioxide-venting pups.

Much of the detailed physiology of gas exchange in sharks has been worked
out using small, captivity-tolerant species such as the Spiny Dogfish (Squalus
acanthias), Lesser Spotted Catshark (Scyliorhinus canicula), and
the Port Jackson Shark (Heterodontus portusjacksoni). Because oxygen's
electron-stealing abilities are so important to powering multicellular
creatures, evolution has conserved shark gas exchange mechanisms, retaining
them with little or no modification. Yet the White Shark has evolved some
fascinating respiratory adaptations that foster its actively predaceous
lifestyle. An intriguing 1986 paper by physiological ecologist Scott Emery
and pathologist Andrew Szczepanski studied gill dimensions in seven species
of active, pelagic sharks including the Great White. They found that the
White Shark has proportionately the longest gill filaments than any other
species they examined. Long gill filaments substantially increase the total
gill surface area per unit of body mass. For example, a 220-pound
(100-kilogram) White shark has a total gill surface area of about 380 square
feet (30 square metres), while a Blue Shark (Prionace glauca) of the same
mass has a total gill surface area of about 150 square feet (14 square
metres) — less than half as much. Emery and Szczepanski concluded that
sharks with relatively large gill surface areas, like the Great White,
increase the total amount of oxygen available to support their high energy
lifestyle.

Blood Characteristics of the White Shark & Selected Other Creatures

Species

Hematocrit

Hemoglobin

White SharkCarcharodon carcharias

26 - 46

25 oz/pt
(14 g/100ml)

HumanHomo sapiens

38 - 42

25 oz/pt
(14 g/100ml)

Bluefin TunaThunnus thynnus

41 - 52

3 - 3.6 oz/pt
(15 - 20 g/100ml)

Blue SharkPrionace glauca

±28

1.4 oz/pt
(8 g/100ml)

Spiny DogfishSqualus acanthias

±19

0.7 oz/pt
(4 g/100ml)

Yet another of the White Shark's adaptations to its high-energy lifestyle
is found in its blood. Blood is composed of two basic types of tissue, cells
and plasma. The percentage of blood volume that is composed of cells is
called hematocrit. The hematocrit of a healthy adult man is about 42, while
that of a healthy adult woman is about 38. In a 1985 paper, Scott Emery
found that hematocrit of a White Shark ranges from roughly 26 to 46,
averaging about 36. As the accompanying table shows, this value is high
compared with other sharks and is on par with that of humans and Bluefin
Tunas (Thunnus thynnus). In addition, Emery found that the amount of
hemoglobin in a White Shark averages at least 2.5 ounces per pint (14 grams
per 100 millilitres) of blood [one of his samples may have been contaminated
with fluid from around the heart]. By comparison, a healthy adult woman has
an average hemoglobin density of about 2.5 ounces per pint (14 grams per 100
millilitres) and a Bluefin about 3 to 3.6 ounces per pint (14 grams per 100
millilitres). Thus, the Great White has blood characteristics closer to that
of humans and highly active teleosts than to most other sharks.